The Evolution of the Tetrapod Middle Ear in the Rhipidistian-Amphibian Transition

AM. ZOOLOGIST, 6-379-397(1966).

The Evolution of the Tetrapod Middle Ear in theRhipidistian-Amphibian Transition

KEITH STEWART THOMSON

Department, of Biology and Penbody Museum, Yale UniversityNew Haven, Connecticut

SYNOPSIS: From a survey ot the structure of the skull in rhipidistian fishes and early laby-linthodont Amphibia and of the mechanism of hearing in these two groups, an account ofthe evolution of the tetrapod middle ear is presented. The overall modification of the oticregion o£ the skull during the rhipidistian-amphibian transition is analyzed in terms ofchanges in different organ systems in response to different selective pressures (affecting, forexample, the feeding, respiratory, and locomotory mechanisms). These changes are seen tooccur in a completely integrated pattern. Considerations of the different requirements forsound reception under water and in air, in connection with this correlated progression ofevolutionary change in the otic region of the head, reveal the manner in which the hyoman-dibular, spiracular diverticulum, and operculum of rhipidistian fishes became modified tolorm the stapes, the tympanic cavity, and the outer portion of the tympanum, respectively,of tetrapods.

The ear in vertebrates consists of twoprincipal portions. The sensory structuresof the inner ear associated with the brainand enclosed within the cranial cavity areessentially comparable in all vertebrates,although developed and modified to vary-ing extents. The nature of the organ bywhich information about sound is conduc-ted to the inner ear is different in fishesand in tetrapods, and this difference resultsfrom a basic difference in the problem ofsound reception under water and on land.In fishes, sound (here we are concernedwith wave-form pressure-disturbances of themedium, rather than seismic disturbances)passes more or less freely through the body-water interface owing to the similarity ofrelative density, and thus acoustic imped-ance, of tissues and medium. In fishes,the receptor organ must include a struc-ture which is opaque to sound waves, andgenerally this is an air-space enclosed withinthe body, usually associated with the air-bladder (see van Bergeijk, 1966, and thisSymposium). The range of different recep-tor organs in fishes is great, but one featurethey have in common is that they need notbe located near the surface of the body. Ina terrestrial animal, the body-air interfaceis a barrier to the sound pressure-field. Thereceptor organ for sound in tetrapod verte-brates (the middle ear), therefore, must

include a specialized surface structure—aflexible membrane (the tympanum)— whichis capable of reacting to the pressure field,a structure (the stapes), or structures, whichcan transmit the vibration of the tympanumto the inner ear organ, and also a specialcavity behind the receptor membrane whichallows the tympanum and stapes to movefreely.

This paper is concerned with the problemof establishing the evolutionary process bywhich the middle ear of tetrapods couldhave evolved from that of fishes. We mustdiscover the morphological and functionalcontinuity which links these apparently en-tirely distinct patterns of middle ear struc-ture.

Classical embryological and morphologi-cal studies have established beyond ques-tion the homology of the tetrapod stapeswith the hyomandibular bone in fishes.This view is so well-known and universallyaccepted that no defense or bolstering isneeded in this study. We may concentrateour attention upon examination of the com-bination of adaptive and selective factorscontrolling the evolutionary transformationof this principal bone in the fish-jaw sus-pension to an element in the tetrapodmiddle ear.

The earliest tetrapods, the Amphibia, asis well known, evolved from ancestral cross-

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380 KEITH STEWART THOMSON

opterygian fish, members of the Rhipidistia,during Devonian time or slightly earlier.The principal characters in this study willthus be the Rhipidistia and the early Palae-ozoic Amphibia. Much of the data pre-sented here concerning the evolutionaryhistory of the Rhipidistia is original andis culled from studies presently being pur-sued or prepared for publication. Withrespect to the Amphibia, I have mainlyconcentrated attention on a single, andhopefully not too atypical, genus, Palaeo-gyrinus, while Professor Olson's paper (thisSymposium) will elaborate the amphibianaspect of the story. Essentially my aim isto discuss the sort of events which occurredduring the rhipidistian-amphibian transi-tion and the sorts of factors controllingthem, rather than to attempt to discussparticular lineages. Our approach must befunctional and morphological rather thansimply systematic.

THE RHIPIDISTIAN FISHES

We may begin by reminding ourselves ofthe basic structure of the skull in rhipidis-tian fishes. The illustrations (Figs. 1 and2) will serve in lieu of a lengthy verbal de-scription. The braincase in Rhipidistia isformed in two separate portions, articu-lating with each other by a well-formedintracranial joint. The palate is attachedto the braincase at only one point, behindthe postnasal wall, where there is a fairlyclose connection of the two elements al-though a small amount of relative move-ment was possible. Otherwise the palate,and therefore also the lower jaws, whichhinge on the quadrate portion of the palato-quadrate, are suspended from the skull onlyby the large separate hyomandibular bone.The skull is thus purely hyostylic: theonly other interconnections of palate andbraincase are through ligaments and theattachment of muscles. The proximal artic-ulation of the hyomandibula onto the pos-terior portion of the braincase is double(Fig. 1) and the arrangement of the two

articular surfaces is of the greatest import-ance in connection with the complicated

kinetic mechanism of the rhipidistian skullwhich involves articulation of the intra-cranial joint (see below). The dermal roofof the skull is also arranged in two com-ponent portions. The anterior portion ofthe roof plus the cheek elements form oneunit, and the posterior portion of the roof,covering the posterior division of the brain-case, forms a second unit. The spiraculargill cleft (Fig. 1) opens at the surface be-tween the dorsal margin of the squamosaland the lateral margin of the posteriorroofing bones of the skull. There was prob-ably a ligamentous binding of the hingebetween cheek and skull roof, and in theregion of the intracranial joint itself theintertemporal, supratemporal, postorbital,and sometimes also the squamosal are ar-ranged with a complicated series of over-lapping flanges the pattern of which is alsoof importance to the operation of the intra-cranial kinesis.

Thus the rhipidistian skull is essentiallycomposed of two units, an anterior unit ofendocranium, dermal bones and palate, anda posterior unit of endocranium and dermalroofing bones. The two units are mechani-cally and functionally integrated principallyby the hyomandibular bone. Onto the hyo-mandibular are also articulated the oper-cular series of bones, the lower jaw, andthe strongly developed skeleton of the vis-ceral arch, forming the third, fourth, andfifth components of the whole head.

Close examination of the structure of theposterior portion of the endocranium showsthat the double proximal articulation of thehyomandibular spans the lateral commissureof the lateral wall of the braincase. The jug-ular vein passes through the canal formedby the lateral commissure, and the truncushyomandibularis of the seventh cranialnerve emerges from the braincase immedi-ately medial to the lateral commissure. Asmall palatinus VII nerve passes throughthe lateral wall of the braincase near theanterior opening of the jugular canal, andthe truncus hyomandibularis emergesthrough the posterior opening, curving lat-erally to enter a canal in the body of thehyomandibular bone. It gives off an oper-

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ORIGIN OF TETRAPOD MIDDLE EAR 381

FIG. 1. Lateral view of the skull of Ectosteorhachis.A, dermal bones. B, dermal bones removed. C,dermal bones and palatoquadrate removed, bp,basipterygoid process; es, extrascapular; £b, fossabridgei; fh, facets for proximal hyomandibulararticulation; h, hyomandibular; icj, intracranialjoint; it, intertemporal; j , jugal; jc, jugular canal;1, lachrymal; lc, lateral commissure; mx, maxilla;

nc, nasal capsule; op, operculum; op pr, opetcularprocess; p, parietal; pm, premaxilla; po, postorbital;pop, preopercular; pp, postparietal; pq, palato-quadrate; q-j, quadrato-jugal; so, supraorbital; sop,subopercular; sp, spiracle; sq, squamosal; st, supra-temporal; t, tabular; II, optic nerve foramen; V,fifth cranial nerve foramina; VII, seventh cranialnerve foramina.

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382 KEJTH STEWART THOMSON

rop

FIG. 2. Lateral view of otic region of Ectosteo-rhdchis skull. A, dermal bones and palatoquadrateremoved. B, showing inner ear cavity and outlineof hyomandibular. esd, external opening of spirac-ular diverticulum; is, internal opening of spirac-ular cleft; 1, lagena; lat, foramen for ramus lateralisVH nerve; pal, ramus palatinus VII nerve; prf,foramen for profundus V nerve; rk, ramus hyoideusVII nerve; nn, ramus mandibularis VII nerve; rop,ramus opercularis VII nerve; s, sacculus; u, utricu-lus; VIIF, eighth cranial nerve.

cular ramus through a foramen in theposterior wall of the hyomandibular, medialto the opercular articulation, and the hy-oid and mandibular rami emerge togetherthrough a foramen in the anterior wall,distal to the opercular articulation (Fig. 2).

The inner ear in Rhipidistia is quite wellknown from descriptions of Ectosteorhachis,Eusthenopteron, and Osteolepis. As shownin Figure 2, the three semicircular canalsare perfectly formed, and saccular, utricu-lar, and lagenar regions may also be dis-tinguished. The inner ear is located in themidsection. of the posterior endocranium,and the ventral proximal hyomandibulararticulation lies immediately outside thesacculus.

We should note that a complete set ofaquatic respiratory structures—gills, oper-

culum, spiracle, and spiracular sense organ—is present in Rhipidistia. Thus, eventhough the Rhipidistia were almost surelyable to breathe air (there is, of course, nodirect evidence of this), it must be empha-sized that they were primarily aquatic ani-mals. In this connection the spiracular gillcleft bears close attention. It opens inter-nally behind the parasphenoid, between thepalate and hyomandibular. It passes dorsal-ly between the last-named elements andopens as a slit on the surface of the skullas noted above. An unusual feature is thatthis external spiracular opening leads intoa wide pouch—the spiracular diverticulum(Jarvik, 1954) developed dorso-medial tothe dorsal margin of the palatoquadrateand lying against the anterior surface ofthe hyomandibular (Fig. 2). From thisspiracular diverticulum, a small blindpocket reaches anteromedially and surelycontained a spiracular sense organ lyingagainst the lateral wall of the braincase,as seen also in Polypterus, Amia, etc. Al-though the function of the spiracular senseorgan (whose embryological derivation inRecent forms is from a modified neuromastof the lateral sensory system) is not knownthere is no reason to believe that it is di-rectly associated with the development ofthe spiracular diverticulum, for the latterstructure seems only to be developed inRhipidistia. The spiracle itself, in Rhipi-distia, probably served a normal functionas the inhalant aperture for the water cur-rent during respiration. A possible func-tion for the spiracular diverticulum isdiscussed below.

As mentioned above, the hyomandibularis one of the most important elements inthe hyostylic rhipidistian skull. It supportsthe upper and lower jaws (at the quadratearticulation), the skeleton of the visceralarch (hyoid articulation), and the opercu-lum (opercular articulation) and has adouble proximal articulation onto thebraincase. The detailed nature of the intra-cranial kinetic mechanism of Rhipidistia,with which the hyomandibular is so inti-mately bound, is quite complex and formsthe subject of a more comprehensive study

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now in preparation by the author. How-ever, the general nature of the mechanismmust be summarized here for it is of primeimportance in understanding the nature ofthe changes which occur in the otic regionof the skull during the evolutionary transi-tion between fish and tetrapod.

The intracranial kinesis is best describedas a specialization of the feeding and respir-atory mechanism. Essentially it involves adorsal and ventral flexure of the anteriorportion of the endocranium upon the pos-terior portion. This flexure of the intra-cranial joint is operated by a complex seriesof muscles among which the subcephalicmuscles are most important. The move-ments of the tip of the snout in the verticalplane are not accompanied by movementsof the cheek in the same plane, but bymovement of the whole suspensorium inthe horizon Lai plane. As summarized inFigure 3, when the tip of the snout is raisedthe suspensorium is moved forwards andoutwards, and when the snout is depressedthe suspensorium is moved backwards andinwards. These lateral movements of thesuspensorium are controlled and directedby the hyomandibular bone which rotatesin an essentially horizontal arc around itsproximal articulation. The orientation ofthe double proximal articulation ensuresthat this arc is horizontal, and the settingof the hyomandibular at an angle of about45° to the antero-posterior axis of the bodyallows significant vertical displacement ofthe tip of the snout and change in theangle of the upper jaws to the horizontal tobe achieved with surprisingly little antero-posterior movement of the suspensorium(Fig. 4).

HEARING IN THE RHIPIDISTIA

Dr. van Bergeijk has distinguished twodifferent types of 'hearing' phenomena infishes. First, all are equipped for receptionof what van Bergeijk terms near-fie Id sound(water displacements) through the functionof the lateral line system as a single unit.Secondly, many fishes are capable of far-field hearing (reception of pressure waves).

Since the body tissues of fishes are of ap-proximately the same relative density asthe surrounding medium, the receptor or-gan for far-field sounds is always an enclosedair space connected with the swim-bladder/lung or with accessory air-breathing organs(van Bergeijk, 1966, and this Symposium).Our problem here is to determine whatevidence there is that the Rhipidistia werestructurally adapted for the reception offar-field sound.

It is possible that the Rhipidistia pos-sessed some modification of the lungs, per-haps a series of ligaments connecting to theotic region of the skull in the manner ofRecent ostariophysian fishes, that couldhave acted as a far-field receptor. However,there is no evidence for this from our fossilmaterials (the vestibular fontanelle in thelateral otic wall of Eusthenopteron de-scribed by Jarvik (1954) is seen from theaccount of Stensio (1963) not to be asso-ciated with the inner ear organs, and is cer-tainly unknown in any other rhipidistianmaterial; cf. van Bergeijk, 1966). In theabsence of concrete information about re-ceptor organs of this type it seems pre-ferable to concentrate our attention on thehyomandibular bone and associated struc-tures, for it is reasonable to assume that thetransformation of the rhipidistian hyoman-dibular to the tetrapod stapes must haveinvolved a certain continuity of function,that is, that the hyomandibular in Rhipi-distia was connected in some way with arudimentary far-field hearing function. Atfirst sight, the important role that the hyo-mandibular plays in the hyostylic intercran-ial kinesis of Rhipidistia would seem to pre-clude such a function, except perhaps bydirect seismic transmission of vibration ifthe fish were lying on the bottom. However,there are two possibilities which bear closeexamination; both concern the presumedair-breathing capabilities of the Rhipidistia.The first possibility is that an air bubbleheld under the medial surface of the oper-culum would be ideally situated so thatoscillations in its volume in response towave-form pressure-disturbances of thewater could be transmitted as vibrations

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FIG. 3. Mechanical arrangement of the rhipidistianskull. A, resting position, lateral view. B, dorsalflexure of snout (open lines) from resting position(solid lines), lateral view. C, ventral flexure ofsnout (open lines) from resting position (solid

through the hyomandibular (onto whichthe operculum is hinged) and thus to theinner ear. In my laboratory I have observedthat the brachyopterygian fish, Polypterus,(the general structure of which is remark-ably similar to that of Rbipidistia) will veryoften release a small air bubble behind theoperculum upon being disturbed with aglass rod. This is not to say that Polypterushabitually or facultatively keeps an airbubble behind the operculum (this mightinterfere with normal water passage over thegills) for the subject needs much closerattention. However, it is not difficult tosee that even casual retention of an airbubble in this region might bestow a con-siderable immediate advantage in "hear-ing," and that this might easily become in-corporated into the behavior of the fishif the selective advantage were also high.It will be seen that a similar mechanismmight have application in the Dipnoi whichotherwise seem ill-equipped- for far-fieldhearing. It may be noted that in both Dip-noi and Brachyopterygii the exhalant aircurrent during aerial respiration seemsnormally to pass through the mouth, butonce a new gulp of air has been taken, smallbubbles (excess air?) always pass from be-hind the operculum/r suggestirig that thegill chamber is at least temporarily filledwith air. This is, of ̂ course, conjectural andis presented solely with the aim of showinga possible situation, not necessarilyr anactual one.

The second'possibility concerns the spir-acular diverticulum for, as van Bergeijkhas recently indicated (1966), if this cavitywere air-filled, its location next to the hyo-mandibular and the structures of the innerear makes it theoretically an excellent re-ceptor of far-field - sound. At first sight itis difficult to see how this cavity might be-come air-filled since it is essentially externalin location and the spiracle in fishes is norm-

lines), lateral view, D, dorsal view of left side ofskull in positions A, B, and C. x, angle of upperjaw in resting position; y, angle of upper jaw afterdorsal flexure; z, angle of upper jaw after ventralflexure.

ally associated with the respiratory watercurrent. Again, observations on Polypterusgive us a clue to what may have been therhipidistian condition. As was first noted byBudgett, when Polypterus comes to the surf-ace to take air it may occasionally be ob-served to do so through the spiracle, with-out the mouth breaking the surface. Theselective advantage of this is obvious, for itallows the fish to take air with an almost im-perceptible disturbance of the water surface.If this were the case in Rhipidistia, too, wemight postulate that the spiracular diver-ticulum evolved as a sound receptor. Pre-sumably at an early stage the spiracular cleftlacked, the diverticulum hut still possessedthe small recess for the spiracular senseorgan. Casual retention of air in the smallcavity might have been of sufficient selec-tive advantage to trigger a process of ex-pansion of this chamber to a large lateraldiverticulum within which the function ofthe spiracular sense organ, in its own smallpocket, could be separate from the new func-tion of a sound receptor. Dr. van Bergeijkhas suggested an alternate pathway accord-ing to which the initial function of the di-verticulum was as an accessory respiratoryorgan, similar to those of the recent anaban-toids. This seems unlikely in a fish thatalready possessed lungs and gills. Whichevermay be the case, there is strong indicationthat the spiracular diverticulum of Rhipi-distia functioned as an air-filled receptororgan for. fartfield sound.

Neither of the two possibilities just men-tioned would seem to have been directly ofsignificant value to the fish if it were toventure out of water, for the air space con-cerned would be masked from air-bornepressure waves by the tissue-air interface.This problem is discussed at length below.

THE EAR REGION IN LABYRINTHODONTS

In order to examine the manner in which

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psp

FIG. 4. Lateral view of the skull ot Palaeogyrinus.A, dermal bones. B, dermal bones removed. C,dermal bones and palate removed. (Redrawn fromPanchen, 1964.) at, anterior tectal; bo, basioccipi-tal; eo, exoccipital; Co, foramen ovale; it, inter-temporal; j , jugal; 1, lachrymal; mx, maxilla; n,nasal; op, opisthotic; p, parietal; ps, postfrontal;pm, premaxilla; po, postorbital; pit, prefrontal;

pro, pro-otic; psp, parasphenoid; q, quadrate: qj,quadrato-jugal; sph, sphenethmoid; sq, squamosal;st, supratemporal; t, tabular; t fac, tabular facet;V pr, foramen for profundus V nerve; I, II, III,IV, V, VI, foramina for olfactory, optic, third,fourth, fifth, and sixth cranial nerves; VII pal,foramen for rainus palatinus VIT nerve.

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the various rhipidistian structures becamemodified during the transition from fish toamphibian, culminating in the evolution ofthe tetrapod middle ear and the evolutionof the tetrapod faculty of "hearing" wavesounds due to aerial pressure, we must firstreview the structure of the otic region ofthe skull in a primitive Palaeozoic amphib-ian. We may use as an example the anthra-cosaur labyrinthodont, Palaeogyrinus. Thishas been chosen because its structure is wellknown, because it is in many ways extreme-ly primitive (retaining a remnant of therhipidistian cranial kinesis in the movablebasipterygoid articulation and a loose con-nection of the posterior portion of thecheek to the skull roof), and because, beingan anthracosaur, it is also most probablyclose in structure to the amphibian ancestorof the Reptilia.

Figures 4 and 5 summarize the basic oticstructure oi Palaeogyrinus. The large fenes-tra ovalis is situated rather towards thecenter of the inner ear. The rod-like stapes(restoration, Fig. 5) has a short dorsalprocess fitting into the fenestra ovalis, thelatter probably being formed in two por-tions, an anterior process (homologous withthe plectrum in Anura?) which butts ontoor may be fused with the parasphenoid, anda posterior process (homologous with theoperculum of Anura?) which fits into thefenestra ovalis. The stapes has a processinserting onto the tympanum (possibly bya cartilaginous extension) and possibly alsoquadrate and hyoid ligaments. These fivepoints of attachment of the stegocephalianstapes have been homologized by Eaton(1939), Romer (1941), and Westoll (1943)with five processes of the rhipidistian hyo-mandibular. The back of the skull laterallyis formed into an otic notch into whichthere is good evidence that the tympanumwas inserted. The jugular vein and facialnerve pass backwards from the endocranialcavity between the dorsal and ventral proc-esses, as may the stapedial (=orbital)artery which in many labyrinthodonts runsthrough the stapes via a stapedial foramen.The chorda tympani (=rhipidistian r. man-dibularis VII) loops behind the stapes and

then turns forward ventral and distal tothe tympanic process, while the hyoid ramusremains behind the level of the quadrateligament. The palate is fused to the squa-mosal and articulates with the braincaseby a prominent movable basal articulation.All traces of the rhipidistian intracranialarticulation are lost from the braincase (inthe Upper Devonian Ichthostegalia a sutureremains in this position) and from the skullroof, but the posterior portion of the cheekplate, as mentioned above, is only looselyattached to the skull roofing elements (seeFig. 4). Although we have no directevidence of its presence, we may be sure thata tympanic cavity enclosed the stapes fromthe fenestra ovalis to the tympanum, andthus a true tetrapod middle ear was formed.

THE EVOLUTION OF AMPHIBIAN STRUCTURES

In structural and functional terms theorigin of the Amphibia lrom the rhipidis-tian fishes presents a complex integratedmosaic. Several different adaptive trends inthe evolution of the Rhipidistia, involvingdifferent structures and different functions,contributed to the development of the am-phibian grade of organization. Our con-cern here is principally with the series ofadaptive morphological changes affectingthe otic region of the skull.

A principal difference between labyrinth-odont Amphibia and Rhipidistia lies in theoverall proportions of the skull: in the evo-lution of the Amphibia there has been aconsiderable increase in the relative lengthof the anterior portion of the skull (thatportion corresponding to the anterior unitof the rhipidistian skull). The adaptivesignificance of this change is probably thatin this way the length of the tooth row,and thus the size of the dental battery, hasbeen increased without an overall increasein the size of the whole skull. It also re-flects an increasing development of whatOlson (1961) terms the "kinetic inertial"system of jaw mechanics and is surely con-nected with the carnivorous/predatorymode of feeding. The Rhipidistia also useda basically kinetic inertial jaw mechanism

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(complicated by the intracranial kinesis;see Thomson, 1966), and trends towardsrelative elongation of the anterior unit ofthe skull may be seen in at least two groups

of Rhipidistia, the Osteolepidae (cf. Osleo-lepis and Gyroptychius) and the Rhizodon-ticlae (for example, in the line, Tristicop-terus, Eusthenopteron, Eusthenodon, and

B

FIG. 5. Lateral view of otic region of braincase ovale; it, interteraporal; jv, jugular vein; oa, orbitalof Palaeogyrinus. A, showing restored stapes, ves- (=stapedial) artery; on, otic notch; p, parietal;sels, and cranial nerves. B, showing position of ppr, posterior process: ql, quadrate ligament; st,(restored) inner ear organ, apr, anterior process; stapes; t, tabular; tmp, position of tympanum; tpr,ct, chorda tympani; dp, dorsal process; fo, foramen tympanic process; VII, seventh cranial nerve.

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FIG. 6. Dorsal view of the skulls of A, Glypto-pomus; B, Osteolepis; C, Gyroptychius; D, Eusthe-nopteron; E, Ichthyostega; F, Palaeogyrinus. (A-E,

Rhizodus). These represent adaptive trendsthat either foreshadow, or more probablyparallel, the evolutionary progression whichgave rise to the Amphibia. Figure 6, byutilizing certain extremes in cranial pro-portions, illustrates the basic sort of phy-letic progression that must have been in-volved. It is easy to see that an increase inthe size of the dental battery and generalfeeding mechanism could not be achievedby relative enlargement of the posterior unitof the skull without drastic alteration ofthe proportions of the whole body. Tomaintain the hyostylic structure of the skullwould necessitate a hyomandibular of largeand extremely unwieldy size which mightpreclude any great increase in the absolutesize of the fish. The constancy of overallbodily proportions in the rhipidistian fishes,except with respect to the depth of thetrunk which may be relatively greater insome holotychioids, is quite remarkable.Predictably, this constancy of proportion

redrawn from Jarvik; F, redrawn from Panchen)Postparietals shaded.

imposes some restriction on possible changesin the cranial proportions and any suchchange will also affect the nature of the in-tracranial kinesis. Thus, in general, elonga-tion of the anterior unit, if the overall pro-portions of the skull are maintained, leadsto a corresponding reduction of the anglethrough which the anterior unit may bemoved. This is shown in Figure 7 and con-sidered in greater detail in my study ofthe whole system (Thomson, 1966). It isalso demonstrated in a crude way by theprogressive reduction in the size of thearticular surface of the basipterygoid artic-ulation in the rhipidistian genera, Rhizo-dopsis (short snout), Osteolepis (mediumlength snout), Eusthenopteron (long snout);see descriptions by Save-Soderbergh (1936),Thomson (1965), and Jarvik (1954), re-spectively. Obviously, there must have beena critical point beyond which elongationof the snout rendered obsolete the rhipidis-tian intracranial articulation, and this, to-

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FIG. 7. Diagram of the mechanics of the rhipidis-tian skull showing the effect of successive migrationbackward of the position of the intracranial joint

gether with factors associated with increasein absolute size and the mechanical prob-lems of suspending a disproportionatelylarge anterior unit upon a small posteriorunit of the skull, led to the abandonmentof the hyostylic suspension of the jaw. Fu-sions of the palate to the cheek and thecheek to the skull roof then followed (inanthracosaurs the loose cheek-skull roofattachment was supplemented by dynamicsupport from the large depressor mandibu-lae muscles; see below; Panchen, 1964, andThomson, 1966). Thus, we may see asequence by which, from changes in thefeeding mechanism, the hyomandibularbone was freed from part of its supportivefunction. Furthermore, once this had hap-pened, the way became more clear for theposition of the quadrate to be pushed back-wards from its rhipidistian position, thuseven further extending the size of the gap.The posterodorsal margin of the squamosalthen comes to form the lower margin ofthe newly-forming otic notch (note thatmany authors seem to have assumed thatthe quadrate actually moved forward in thefish-amphibian transition). However, thisposterior extension of the suspensoriumcould not occur without progressive modifi-cation of the respiratory mechanism, es-pecially the operculum.

Although changes in the respiratorymechanism involve many of the same fea-

(1, 2, 3) upon the angle through which the snoutmay be deflected (1', 2', 3', lespectively) for agiven movement of the hyomandibular.

tures of the otic region of the skull as dochanges in the feeding mechanism, theyoccur in response to an entirely differentseries of selective pressures, involving theadoption of aerial respiration as the princi-pal method of respiration in adult Am-phibia. Essentially, with increasing depen-dence on the lungs for respiration, theoperculum, skeleton of the visceral arches,and the muscles associated with them, be-come superfluous. Their progressive modi-fication or reduction removes the last sup-portive function of the hyomandibular. Ab-sence of these structures also releases spacefor the reorganization of the otic anatomy,as noted below. There is little evidence thatloss of the operculum occurs in responseto a requirement for increasing lateral mo-bility of the head upon the trunk (Westoll,1943); this seems to be a by-product whichis not of significant utility until the am-phibians have considerably less dependenceupon the aquatic environment for loco-motion and feeding. A most important fac-tor in the reorganization of the otic anato-my necessitated by loss of the gills andoperculum is that from the embryonic hyoidconstrictor muscle sheath, from which themuscles of the hyomandibular and opercu-lum of fishes are formed, new mandibulardepressor muscles, which are necessary forthe operation of the elongate and heavylower jaws, may be formed. Dorsally, these

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new muscles have their origin in the epax-ial fascia and on the posterior surface ofthe tabular bone. The posterior extensionof the tabular for their support contributesin part to the formation of the dorsal mar-gin of the otic notch, as does loss of theextratemporal and supracleithral dermalbones. Furthermore, from the modifiedhypobranchial muscles is formed the buccalpump by which the lungs are filled. TheDipnoi, which are also air-breathing, atleast in part, show an exactly comparablereduction of gill structures and modificationof the muscles.

The structural and functional integra-tion of the changes occurring in response tomodifications of the feeding and respira-tory requirements is most remarkable, andto it may be added changes in a third sys-tem, namely, the support of the head uponthe trunk. In crossopterygian fishes thiswas not a great problem since the water-medium, and to some extent the noto-chord, supplied most of the vertical sup-port necessary. Moreover, the otic region ofthe skull in Rhipidistia bears a pair ofdorso-lateral excavations, the fossae bridgei,into which the epaxial musculature in-serted. Presumably, this strong insertion,which undoubtedly contributed to the verti-cal support of the head, was connected pri-marily with the strong lateral forces de-veloped during powerful swimming move-ments. In primarily aquatic amphibianssuch as Palaeogyrinus, these muscles havestrong insertions on the medial faces of thetabular horns since the fore-shortening ofthe otic region of the skull essentially ob-literates the fossae bridgei. In other Am-phibia which seem to have been more ter-restrial in habit, such as the Rhachitomi,lateral and vertical movement of the headupon the trunk would have been impededby tabular horns, and the epaxial muscula-ture is inserted on the occipital face of theskull in post-temporal fenestrae which seemdirectly homologous with the fossae bridgeiof fishes. This matter of insertion of theepaxial muscles is,'another factor affectingthe shape of the otic notch.

From this series of integrated changes

(which no doubt includes many factors yetto be recognized) the tetrapod ear emerged.The integration of these changes must havebeen complete, that is, it must have beenstructural, functional, and temporal (Fig.8) in a system of correlated progression. Thewhole progression is more or less related tothe occupation of a more "terrestrial" habi-tat or, rather, to a decreasing dependenceupon the aquatic environment either forfeeding or breathing. A part of the generalselective pressure must have been towardthe perfection of a hearing organ thatcould operate effectively both in the waterand out. In the preceding paragraphs anattempt has been made to demonstrate thestructural and functional continuity main-tained during the transformation of thegeneral otic anatomy during the rhipidis-tian to amphibian transition. It is nownecessary to examine this process more close-ly to discover whether the same continuitymay be seen in the evolution of the tetra-pod middle ear (the stapes, tympanum, andtympanic cavity).

The development of aerial hearing intetrapods.

As we have already noted, underwaterhearing requires the presence of an air-space within the body cavity of the fish.In response to changes in pressure of soundwaves propagated through the water andthrough the tissues of the fish, the volumeof this air cavity varies. The physical dis-placement of the walls of the cavity is trans-mitted through the tissues of the fish (some-times by special structures, such as theWeberian ossicles) and received by theinner ear organs. Thus, underwater hearingin a fish is a process depending upon thevolume/pressure relationships of an en-closed air space which produces a particulartype of mechanical displacement in responseto a given sound. Once the fish leaves thewater this situation is completely changed,and the air space is masked from the air-borne sound waves by the surroundingbody tissues (by virtue of the difference inacoustical impedance of tissue and air).

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hyomandibular

suspensorium

spiracular

'diverliculum

operculumFIG. 8. Two-dimensional representation of the correlated changes leading to the developmentof the tetrapod middle ear.

Thus, a new way must be found to de-velop a mechanical response to the pressurechanges which constitute the sound wave.The problem is solved by greatly specializ-ing a region of the body surface in such away that it is physically capable of regis-tering the tiny changes in air pressure interms of slight mechanical deformationswhich are transmitted to the inner earorgans. Clearly, in addition to this special-ized surface structure, a specialized trans-mitting organ is required—the ear ossicle.The specialized surface membrane (thetympanum) and the ear ossicle (the stapes)must also be freely suspended within thebody in order that the small movementsdeveloped in the tympanum may be trans-mitted to the inner ear with maximummechanical efficiency. This is accomplishedby enclosing the whole organ in an' airspace—the tympanic cavity. From what wehave already seen of the structure of rhipi-distian fishes and amphibians, it is obviousthat the tetrapod stapes has evolved from

the hyomandibular of fish, and the tym-panic cavity must be related to the spirac-ular diverticulum. Further, if our attribu-tion of an underwater hearing function tothe hyomandibular is correct, then there isnot only a morphological, but also a func-tional, continuity between the two sets ofstructures in fish and amphibia.

van Bergeijk (this Symposium) has de-veloped an ingenious theoretical modelwhich seeks to interpret this continuity.According to his theory, the same pressure/volume relationships which determine thecharacteristic response of the "middle ear"of fish are also of vital importance in theterrestrial vertebrates. However, since asound in air "produces only 1/63 of thepressure developed by an underwater sourceof the same intensity" (van Bergeijk, thisSymposium);, then,, he believes, some devicehas to be found by which the displacementof the wall of the air-space could be in-creased by 63 times. This, he suggests,could be accomplished by restricting the

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movable portion of the wall of the cavityto 1/63 of the total surface area. This re-stricted surface, necessarily coming to thebody surface, becomes the tympanum. Un-fortunately, closer examination of thistheory shows that it is incompatible withmost of what we know about the practicalsituation. First of all, van Bergeijk's modelis made with the assumption that all theenergy that would be available to the cavityif the whole of its wall were flexible (asis the case when the fish is under water)is still available in air when only 1/63 ofthe surface is movable. However, this isnot the case. The tetrapod tympanum isnot moved from within, it is moved fromthe outside. Thus, since the force availablefor deformation of the wall of the tympaniccavity is proportional to the surface areaupon which the pressure acts (pressure =force per unit area), in the model only1/63 of the force is available. Clearly then,it is desirable that the tympanum, the onlyplace upon which the sound pressure canact, should really be as large as possiblein order to produce the optimum responseto a sound of given characteristics.

Secondly, in his theoretical model theassumption is made that the tympanum isnot loaded. However, in fact, the tympan-um is connected to a large and relativelyextremely heavy hyomandibular (especiallyin the earliest stages of the transition). Nowaccording to the equation, F (force) = M(mass) X a (acceleration), the addition ofthe hyomandibular (stapes), which couldscarcely have a mass less than 20 timesthat of the tympanum itself, to the tympan-um will reduce the acceleration which maybe produced by a corresponding proportion.This is a second factor favoring increase inthe size of the tympanum.

The next question is: suppose that thesurface area of the tympanum were to beincreased beyound the theoretical 1/63 pro-portion, would the change in volume whichits displacement produces be greater thancould be accommodated by the tympaniccavity, the walls of which (according to vanBergeijk) are essentially inflexible? Herewe encounter a third objection to the pro-

posed theoretical model. Simply considerthe tympanic cavity of a large specimen ofa rhipidistian fish such as Eusthenopteron:it might have had a volume of about 4 cm3,that is, a volume equivalent to that of asphere with radius of 1.0 cm. Now a typicalmovement of the tympanum of a tetrapodmight be expected to be in the vicinity of10 A (1 X 10"7 cm). If the whole surfaceof the cavity were to be displaced by thisamount, then the total change in volumewould be only 2.57 X 10~T cm3. which isan extremely small amount. However, ifonly 1/63 of the total surface area can move,then the change in volume is now only 4.08X 10"9 cm3. It will be obvious that thisextremely small change is unlikely to havebeen of great significance to the living ani-mal (for example, the pulsing of the sta-pedial artery, which passes through thecavity, would have produced a change involume of this order, or even greater).Clearly then, the surface area of the tym-panum could be increased beyond the 1/63limit many times without significantly af-fecting the pressure/volume relations of thetympanic cavity. We can only concludethat the direct relationship between thepressure and volume of the tympanic cavityand the displacement of the tympanum isnot likely to have been the critical factorin determining the nature and course ofevolution of the tetrapod ear.

From the above considerations we maycome to certain conclusions about the na-ture of the transition as it applies to themechanics of the ear and the physics ofhearing in air. From the two equations,P = F/A (pressure = force per unit area)and F = Ma (force = mass X accelera-tion), and from the fact that for a givensound the acceleration produced will beproportional to (the square of) the fre-quency, there will be an inverse relation-ship between the mass of the tympanum-ear ossicle system and the frequency of thesound that may be received (that is, thatwill produce a given movement of the ossi-cle). If the mass of the ear ossicle is largeand the surface of the tympanum is verysmall, the range of possible frequency re-

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sponse is extremely limited. Frequency re-sponse could only be greater if the intensityof the sound were greater, that is if thepressure acting upon unit tympanic areawere greater. However, we are talking hereof an evolutionary process. All that weknow about such processes requires us toexpect that through even the very earlieststages of evolution the ear must have hadsignificant functional value. In this casethe animal must have been capable of re-sponding to a useful (if small) range offrequencies, (e.g., up to 150-200 cps) atrelatively modest intensities (an equivalentof ca. 60-80 decibels). An inescapable factabout the hyomandibular in the fish-am-phibian transition is, as we have seenabove, that it has important connections tothe palatoquadrate bones, the lower jaw,the visceral skeleton, and to the operculumwhen present, together with various liga-ments and muscles. Thus the effective massof the ear ossicle in the transitional stageswas extremely high, and the mechanicalwork that had to be performed in orderto accelerate the stapes, even over the shortdistance of 10 A, is also considerable. Sincethe energy that is available to do the workis solely that which is "received" by thetympanum, we must expect the tympanum,at the earliest stages, to be of large size. Thisis especially true when we consider thatin the earliest stages the tympanum may beexpected to be relatively unspecialized instructure, van Bergeijk has pointed out tome (personal communication) that theproblem of matching impedance is takencare of by matching the mass of the hyo-mandibular to that of the inner ear. Inthis connection it is interesting to notethat the oval window is not perforate untilthe full amphibian condition is reached, atwhich time the hyomandibular (stapes) isrelatively much less massive.

There is, of course, a possibility that themovement of the hyomandibular was am-plified by mechanical leverage as the bonewas moved about its fulcrum at the dorsalproximal articulation. This amplificationis unlikely to have been greater than afactor of 2.

We may now turn to examine the morph-ology of the rhipidistian fishes to determinefrom what structure the amphibian tym-panum has evolved.

Arguing from the basis of his theoreticalmodel (the validity of which has beenquestioned above) van Bergeijk has de-veloped the theory (this Symposium) thatthe rhipidistian fish possessed a rudimentarytympanic membrane in the region ofthe spiracular opening, the membrane be-ing formed by the pressing of the outerwall of the spiracular diverticulum againstthe ligament binding the squamosalto the tabular. There are certain practicaldifficulties in this theory, the principal onebeing that the connection between the skullroof and cheek plate must have been veryclose, the only significant gap being in thenotch between the tabular and supratemp-oral where the spiracle opens. Most proba-bly the squamosal-tabular contact was asimple hinge at which the squamosal wasable to rotate upon the tabular while re-maining in contact with it. The two boneswere bound together by a ligamentous con-nection, but it is unlikely that, even dur-ing movements of the cheek associated withthe cranial kinesis, the two bones were everseparated by more than a millimeter. Inany case, if the fish were to venture on land,the cheek and operculum would surely betightly adducted to prevent drying of thegills; in this position the squamosal andtabular would be pressed firmly together.Thus, it is unlikely that even a rudimentaryeardrum could have developed in thisposition. Even if such a structure were pres-ent, the mechanical requirements of thehinge are such that the ratio of the thicknessof ligament to the width of slit must havebeen very high (in the order of 0.6-0.9 : 1)and the ligament is, therefore, unlikely tohave been physically suited for acting as atympanum. Further, if such a system werepresent it would only be capable of func-tioning as a sound receptor device if thevibrations of the "tympanum" could betransmitted to the otic capsule through thehyomandibular. In the hypothetical tym-panum in EusUienopteron postulated by

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van Bergeijk, the "eardrum" would bebounded solely by the dermal bones of theskull. The hyomandibular does not reachthe opening of the diverticulum or anydermal bone except the operculum (thisis shown clearly by Jarvik, 1954, Fig. 47).The only connection of the hypotheticaleardrum to the hyomandibular is, thus, theflexible medial wall o£ the diverticulumwhich meets the "drum" at its attachmentto the rim of the tabular bone. It does notseem likely that this could serve for anefficient transmission of "tympanic" vibra-tion to the hyomandibular. The main ob-jection to this theory is that such an "ear-drum" would have been far too small tooperate the massive hyomandibular in themanner that we have seen (above) wouldbe necessary for effective functioning of theear.

The only serious candidate as the precur-sor of the tetrapod tympanum seems to bethe opercular bone. We have noted pre-viously that it might have a function inunderwater hearing. It is directly con-nected to the hyomandibular bone, andcomparative anatomical and embryologicalevidence suggests that the connection of theoperculum to the hyomandibular in fishesis homologous with the tympanic process ofthe tetrapod stapes. Briefly, the hypothesismay be presented that in certain rhipidis-tian fishes the selective advantage of beingable to "hear" far-field sound underwaterwould lead to an increase in the size ofthe spiracular diverticulum. Such an in-crease would be facilitated by the generalchanges in the proportions of the skullwhich, among other things, made spaceavailable for this expansion and involveda progressive decrease in the suspensorialfunctions of the hyomandibular. Eventu-ally the spiracular diverticulum would beable essentially to surround the hyomandi-bular, and there would be developed atympanic cavity of the basic tetrapod type.We should note that it would not be ofadvantage for the cavity to enclose thehyomandibular completely unless therewere also developed some mechanical meanswhereby the oscillations in volume of the

cavity could be transferred to the hyo-mandibular. At an earlier stage this wasachieved through contact of the medialwall of the cavity with the hyomandibular.In the most advanced fish-stage this wasbest achieved through a connection of theouter wall of the cavity to a distal part ofthe hyomandibular, and this would occurat the opercular process which naturallylimits the lateral extent of the cavity. Itis theoretically possible that this stage ofdevelopment of the tympanic cavity couldbe attained while a full set of gill struc-tures was still present if the animal wereconcerned only with the underwater hearingand structural modification of the otic re-gion of the skull had otherwise proceededfar enough to allow for expansion of thecavity. This might, then, closely approxi-mate the "prototetrapod" stage that Par-rington (1958) envisioned in the fish-tetra-pod sequence, since the stapes would beonly moderately modified from the rhipidis-tian condition and the otic notch wouldnot be developed. However, the fully-cor-related nature of all the adaptive changesoccurring in the otic region of the skulland the nature of the selective pressuresinvolved indicate that development of atetrapod-type of tympanic cavity was pro-ceeding in step with reduction of the wholeaquatic respiratory system. Thus, we maysuggest that precisely as the tympanic cavityexpanded to enclose the hyomandibular andreached out laterally to the opercular proc-ess, the gills were fully reduced. Whenthe fish "came on land" the former opercu-lum, now lying in and being supported bythe new otic notch, became a new andflexible structure which, by virtue of itsshape and large size, was able to vibratedirectly in response to air-borne pressurewaves and to transfer this motion to thehyomandibular (now the stapes, lying inthe tympanic cavity) by way of the opercu-lar (tympanic) process. Since this mechan-ism must at the very outset also have beenrequired to receive water-borne pressurewaves, it is clear that the outer wall of thetympanic cavity must have been closelyapplied to the inner surface of the opercu-

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lum in order that volume changes of theair-filled tympanic cavity would also betransmitted to the stapes via the tympanicprocess. According to this view, the tetra-pod tympanum may be considered to havebeen derived from two sources, the outerportion from the former opercular boneand the inner portion from the wall of thespiracular diverticulum of the fish ancestor.

It might seem that the radical nature ofthese structural modifications, especiallyin the respiratory system, might presentserious problems in the ontogenetic me-chanics of the earliest amphibian larvae.This would not have been so if, as seemsmost probable, the larvae of Rhipidistiapossessed external gills. Indeed, the pres-ence of larval external gills in the ancestralstages is virtually a prerequisite for thewhole evolutionary sequence.

POSTSCRIPT

One point of general theoretical import-ance emerges from this evolutionary studyof the rhipidistian and amphibian oticanatomy. Many authors from Darwin on-wards have observed that selection of aparticular character is frequently accom-panied by correlated side-effects which arenot directly related to the immediate se-lective pressure or the particular structureupon which the selection is apparently act-ing. These responses have been called "cor-related responses" or "correlated effects"(see Mayr, 1963, pp. 287, 290, 607). The se-quence of events which I have called "cor-related progression" above is clearly relatedto these effects but in a curious and specialway. In a correlated progression of evolu-tionary change, such as we have seen tohave been associated with the origin of thetetrapod middle ear, correlated changesoccur in related structures in response todifferent selective pressures. The progressof each modification is dependent upon thesimultaneous progress of the other modifi-cations and the whole system may be con-sidered to act in response to an overallselection which is the sum of the series ofseparate pressures and responses (concern-ing feeding, respiration, locomotion, etc.).

In the example considered here, this overallselection is concerned with decreasing de-pendence upon the aquatic habitat and hasresulted in the origin of an entirely neworgan, the tetrapod middle ear. The impli-cation of this sort of analysis of palaeonto-logical data is considerable, having bear-ing upon such subjects as preadaptationand the mechanism of the origin of majorgroups, but consideration of these mattersmust be made elsewhere than in the presentpaper.

Finally, on a phylogenetic note, it willbe recognized that in the preceding pagesI have been concerned principally with theevolution of the labyrinthodont middle ear.My study of this leads me to the conclusionthat from the outset an important factorin the evolutionary complex is the develop-ment of an otic notch and also a relativelydorsal position of the stapes. Thus, if theReptilia have evolved from a labyrintho-dont ancestor, the stapes must have mi-grated ventrally from an originally dorsalposition (see Parrington, 1958, 1959; Hot-ton, 1959, 1960). If the Amphibia are trulymonophyletic, then all early forms musthave possessed an otic notch and dorsalstapes. However, it is perfectly possible thatvarious Palaeozoic Lepospondyli have hada separate origin (cf. Thomson, 1964; Rom-er, 1964; Schaeffer, 1965) and could have de-veloped an essentially homologous middleear by a slightly different pathway; in thisline, modification of the feeding mechanismmay not have involved a posterior migra-tion of the quadrate.

ACKNOWLEDGMENTS

The final version of this paper was prepared afterthe Symposium for which it was originally written,and after extended discussion of the topic with Dr.W. A. van Bergeijk whose own contribution pre-sents a different viewpoint on the origin of thetympanum. I wish to thank Dr. van Bergeijk andalso Dr. J. A. Hopson for valuable discussions onthis subject. Thanks are also due to my wife andto Ivfrs. Barbara E. Moss for assistance with thepreparation of the manuscript.

REFERENCES

Eaton, T. H. 1939. The crossopterygian hyoman-dibular and the tetrapod stapes. J. Washington

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Acad. Sci. 29:109-117.Hotton, N. 1959. The pelycosaur tympanum and

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The Evolution of the Tetrapod Middle Ear in the Rhipidistian-Amphibian Transition

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